Life in a rock pool: Radiation and population genetics of myxozoan parasites in hosts inhabiting restricted spaces
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
29561884
PubMed Central
PMC5862482
DOI
10.1371/journal.pone.0194042
PII: PONE-D-17-40287
Knihovny.cz E-zdroje
- MeSH
- fylogeneze MeSH
- interakce hostitele a parazita genetika fyziologie MeSH
- Myxozoa klasifikace genetika MeSH
- nemoci ryb parazitologie MeSH
- parazitární nemoci u zvířat parazitologie MeSH
- paraziti klasifikace genetika MeSH
- populační genetika metody MeSH
- ribozomální DNA genetika MeSH
- ryby parazitologie MeSH
- stadia vývoje genetika MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Geografické názvy
- Jihoafrická republika MeSH
- Názvy látek
- ribozomální DNA MeSH
INTRODUCTION: Intertidal rock pools where fish and invertebrates are in constant close contact due to limited space and water level fluctuations represent ideal conditions to promote life cycles in parasites using these two alternate hosts and to study speciation processes that could contribute to understanding the roles of parasitic species in such ecosystems. MATERIAL AND METHODS: Gall bladder and liver samples from five clinid fish species (Blenniiformes: Clinidae) were morphologically and molecularly examined to determine the diversity, prevalence, distribution and host specificity of Ceratomyxa parasites (Cnidaria: Myxozoa) in intertidal habitats along the coast of South Africa. Phylogenetic relationships of clinid ceratomyxids based on the SSU rDNA, LSU rDNA and ITS regions were assessed additionally to the investigation of population genetic structure of Ceratomyxa cottoidii and subsequent comparison with the data known from type fish host Clinus cottoides. RESULTS AND DISCUSSION: Seven Ceratomyxa species including previously described Ceratomyxa dehoopi and C. cottoidii were recognized in clinids. They represent a diverse group of rapidly evolving, closely related species with a remarkably high prevalence in their hosts, little host specificity and frequent concurrent infections, most probably as a result of parasite radiation after multiple speciation events triggered by limited host dispersal within restricted spaces. C. cottoidii represents the most common clinid parasite with a population structure characterized by young expanding populations in the south west and south east coast and by older populations in equilibrium on the west coast of its distribution. Parasite and fish host population structures show overlapping patterns and are very likely affected by similar oceanographic barriers possibly due to reduced host dispersal enhancing parasite community differentiation. While fish host specificity had little impact on parasite population structure, the habitat preference of the alternate invertebrate host as well as tidal water exchange may be additional crucial variables affecting the dispersal and associated population structure of C. cottoidii.
Department of Biological Sciences University of Cape Town Rondebosch South Africa
Faculty of Science University of South Bohemia in České Budějovice České Budějovice Czech Republic
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Huggett J, Griffiths CL. Some relationships between elevation, physicochemical variables and biota of intertidal rock pools. Mar Ecol Prog Ser. 1986;29(2): 189–197.
Bennett BA, Griffiths CL. Factors affecting the distribution, abundance and diversity of rock-pool fishes on the Cape Peninsula, South Africa. S Afr J Zool. 1984;19(2): 97–104.
Prochazka K, Griffiths CL. The intertidal fish fauna of the west coast of South Africa—Species, community and biogeographic patterns. S Afr J Zool. 1992;27(3): 115–120.
Teske PR, von der Heyden S, McQuaid CD, Barker NP. A review of marine phylogeography in southern Africa. S Afr J Sci. 2011;107(5–6): 43–53.
von der Heyden S, Lipinski MR, Matthee CA. Remarkably low mtDNA control region diversity in an abundant demersal fish. Mol Phylogenet Evol. 2010;55(3): 1183–1188. doi: 10.1016/j.ympev.2009.09.018 PubMed DOI
von der Heyden S, Bowie RCK, Prochazka K, Bloomer P, Crane NL, Bernardi G. Phylogeographic patterns and cryptic speciation across oceanographic barriers in South African intertidal fishes. J Evol Biol. 2011;24(11): 2505–2519. doi: 10.1111/j.1420-9101.2011.02382.x PubMed DOI
Muller CM, von der Heyden S, Bowie RCK, Matthee CA. Oceanic circulation, local upwelling and palaeoclimatic changes linked to the phylogeography of the Cape sea urchin Parechinus angulosus. Mar Ecol Prog Ser. 2012;468: 203–215.
Lin HC, Hastings PA. Phylogeny and biogeography of a shallow water fish clade (Teleostei: Blenniiformes). BMC Evol Biol. 2013;13: 18 doi: 10.1186/1471-2148-13-18 PubMed DOI PMC
Stepien CA. Evolution and biogeography of the Clinidae (Teleostei, Blennioidei). Copeia. 1992(2): 375–392.
Wright D, Bishop JM, Matthee CA, von der Heyden S. Genetic isolation by distance reveals restricted dispersal across a range of life histories: Implications for biodiversity conservation planning across highly variable marine environments. Diversity and Distributions. 2015;21(6): 698–710.
von der Heyden S, Prochazka K, Bowie RCK. Significant population structure and asymmetric gene flow patterns amidst expanding populations of Clinus cottoides (Perciformes, Clinidae): Application of molecular data to marine conservation planning in South Africa. Mol Ecol. 2008;17(22): 4812–4826. doi: 10.1111/j.1365-294X.2008.03959.x PubMed DOI
von der Heyden S, Gildenhuys E, Bernardi G, Bowie R. Fine-scale biogeography: Tidal elevation strongly affects population genetic structure and demographic history in intertidal fishes. Front Biogeogr. 2013;5(1): 29–38.
Holleman W, Von Der Heyden S, Zsilavecz G. Delineating the fishes of the Clinus superciliosus species complex in southern African waters (Blennioidei: Clinidae: Clinini), with the validation of Clinus arborescens Gilchrist & Thompson, 1908 and Clinus ornatus Gilchrist & Thompson, 1908, and with descriptions of two new species. Zool J Linnean Soc. 2012;166(4): 827–853.
Firth LB, Schofield M, White FJ, Skov MW, Hawkins SJ. Biodiversity in intertidal rock pools: Informing engineering criteria for artificial habitat enhancement in the built environment. Mar Environ Res. 2014;102: 122–130. doi: 10.1016/j.marenvres.2014.03.016 PubMed DOI
Astles KL. Patterns of abundance and distribution of species in intertidal rock pools. J Mar Biol Assoc UK. 1993;73(3): 555–569.
Mouritsen KN, Poulin R. Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology. 2002;124: S101–S117. PubMed
Okamura B, Gruhl A, Bartholomew JL. Myxozoan Evolution, Ecology and Development. Cham Heidelberg New York Dordrecht London: Springer; 2015.
Fantham H. Some parasitic Protozoa found in South Africa II. S Afr J Sci. 1919;16: 185–191.
Fantham H. Some parasitic Protozoa found in South Africa XIII. S Afr J Sci. 1930;27: 376–390.
Reed CC, Basson L, Van As LL, Dyková I. Four new myxozoans (Myxosporea: Bivalvulida) from intertidal fishes along the south coast of Africa. Folia Parasitol. 2007;54(4): 283–292. PubMed
Bartošová-Sojková P, Kodádková A, Pecková H, Kuchta R, Reed CC. Morphology and phylogeny of two new species of Sphaeromyxa Thélohan, 1892 (Cnidaria: Myxozoa) from marine fish (Clinidae and Trachichthyidae). Parasitology. 2015;142(5): 660–674. doi: 10.1017/S0031182014001723 PubMed DOI
Ali MA. Ortholinea basma n. sp (Myxozoa: Myxosporea) from Agile klipfish Clinus agilis (Teleostei: Clinidae), light and scanning electron microscopy. Eur J Protistol. 2000;36(1): 100–102.
Smit NJ, Hadfield KA. Marine fish parasitology in South Africa: History of discovery and future direction. Af Zool. 2015;50(2): 79–92.
Eiras J. Synopsis of the species of Ceratomyxa Thélohan, 1892 (Myxozoa: Myxosporea: Ceratomyxidae). Syst Parasitol. 2006:49–71. PubMed
Gunter N, Adlard R. Bivalvulidan (Myxozoa: Myxosporea) parasites of damselfishes with description of twelve novel species from Australia's Great Barrier Reef. Parasitology. 2008;135(10): 1165–1178. doi: 10.1017/S0031182008004733 PubMed DOI
Gunter N, Whipps C, Adlard R. Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience? Int J Parasitol. 2009;39(12): 1395–1405. doi: 10.1016/j.ijpara.2009.04.008 PubMed DOI
Gunter N, Adlard R. Seven new species of Ceratomyxa Thélohan, 1892 (Myxozoa) from the gall-bladders of serranid fishes from the Great Barrier Reef, Australia. Syst Parasitol. 2009;73(1): 1–11. doi: 10.1007/s11230-008-9162-6 PubMed DOI
Gunter N, Burger M, Adlard R. Morphometric and molecular characterisation of four new Ceratomyxa species (Myxosporea: Bivalvulida: Ceratomyxidae) from fishes off Lizard Island, Australia. Folia Parasitol. 2010: 1–10. PubMed
Alama-Bermejo G, Raga JA, Holzer AS. Host-parasite relationship of Ceratomyxa puntazzi n. sp (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Vet Parasitol. 2011;182(2–4): 181–192. doi: 10.1016/j.vetpar.2011.05.012 PubMed DOI
Heiniger H, Adlard RD. Molecular identification of cryptic species of Ceratomyxa Thélohan, 1892 (Myxosporea: Bivalvulida) including the description of eight novel species from apogonid fishes (Perciformes: Apogonidae) from Australian waters. Acta Parasitol. 2013;58(3): 342–360. doi: 10.2478/s11686-013-0149-3 PubMed DOI
Sitjà-Bobadilla A, Alvarez-Pellitero P. Light and electron microscopic description of Ceratomyxa labracis n.sp. and redescription of C. diplodae (Myxosporea Bivalvulida) from wild and cultured Mediterranean sea bass (Dicentrarchus labrax L.). Syst Parasitol. 1993;26(3): 215–223.
Alvarez-Pellitero P, Sitjà-Bobadilla A. Pathology of Myxosporea in marine fish culture. Dis Aquat Organ. 1993;17: 229–238.
Palenzuela O, Sitjà-Bobadilla A, Alvarez-Pellitero P. Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead sea bream Sparus aurata (Pisces: Teleostei) from Spain: Aspects of the host parasite relationship. Parasitol Res. 1997;83(6): 539–548. PubMed
Køie M, Karlsbakk E, Nylund A. The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitol. 2008;55(2): 100–104. PubMed
Evans BS, Sweijd NA, Bowie RCK, Cook PA, Elliott NG. Population genetic structure of the perlemoen Haliotis midae in South Africa: Evidence of range expansion and founder events. Mar Ecol Prog Ser. 2004;270: 163–172.
Teske PR, McQuaid CD, Froneman PW, Barker NP. Impacts of marine biogeographic boundaries on phylogeographic patterns of three South African estuarine crustaceans. Mar Ecol Prog Ser. 2006;314: 283–293.
Tang L. Observations on myxozoans (Myzozoa: Myxosporea) and the spatial and temporal variation in parasite assemblages of the nosestripe klipfish, Muraenoclinus dorsalis Bleeke, 1860 (Perciformes: Clinidae). M.Sc. Thesis, University of Cape Town, Faculty of Science; 2010. Available from: https://open.uct.ac.za/bitstream/handle/11427/6210/thesis_sci_2010_tang_laura.pdf?sequence=1.
Heiniger H, Gunter N, Adlard R. Relationships between four novel ceratomyxid parasites from the gall bladders of labrid fishes from Heron Island, Queensland, Australia. Parasitol Int. 2008;57(2): 158–165. doi: 10.1016/j.parint.2007.11.006 PubMed DOI
Morrison CM, Martell DJ, Leggiadro C, Oneil D. Ceratomyxa drepanopsettae in the gallbladder of Atlantic halibut, Hippoglossus hippoglossus, from the northwest Atlantic Ocean. Folia Parasitol. 1996;43(1): 20–36. PubMed
Rocha S, Rangel LF, Castro R, Severino R, Azevedo C, Santos MJ, et al. Ultrastructure and phylogeny of Ceratomyxa diplodae (Myxosporea: Ceratomyxidae), from gall bladder of European seabass Dicentrarchus labrax. Dis Aquat Organ. 2016;121(2): 117–128. doi: 10.3354/dao03049 PubMed DOI
Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P. The phylogenetic position of Myxozoa: Exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol. 2010;27(12): 2733–2746. doi: 10.1093/molbev/msq159 PubMed DOI
Hartigan A, Estensoro I, Vancová M, Bílý T, Patra S, Eszterbauer E, et al. New cell motility model observed in parasitic cnidarian Sphaerospora molnari (Myxozoa: Myxosporea) blood stages in fish. Sci Rep. 2016;6. PubMed PMC
Castro LR, Austin AD, Dowton M. Contrasting rates of mitochondrial molecular evolution in parasitic diptera and hymenoptera. Mol Biol Evol. 2002;19(7): 1100–1113. doi: 10.1093/oxfordjournals.molbev.a004168 PubMed DOI
Eo SH, DeWoody JA. Evolutionary rates of mitochondrial genomes correspond to diversification rates and to contemporary species richness in birds and reptiles. Proc R Soc Lond B Biol Sci. 2010;277(1700): 3587–3592. PubMed PMC
Fiala I. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol. 2006;36(14): 1521–1534. doi: 10.1016/j.ijpara.2006.06.016 PubMed DOI
Fiala I, Hlavničková M, Kodádková A, Freeman MA, Bartošová-Sojková P, Atkinson SD. Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage. Mol Phylogenet Evol. 2015;86: 75–89. doi: 10.1016/j.ympev.2015.03.004 PubMed DOI
Brandt M, Fischer-Blass B, Heinze J, Foitzik S. Population structure and the co-evolution between social parasites and their hosts. Mol Ecol. 2007;16(10): 2063–2078. doi: 10.1111/j.1365-294X.2007.03300.x PubMed DOI
Pal C, Macia MD, Oliver A, Schachar I, Buckling A. Coevolution with viruses drives the evolution of bacterial mutation rates. Nature. 2007;450(7172): 1079–1081. doi: 10.1038/nature06350 PubMed DOI
Papkou A, Gokhale CS, Traulsen A, Schulenburg H. Host-parasite coevolution: Why changing population size matters. Zoology. 2016;119(4): 330–338. doi: 10.1016/j.zool.2016.02.001 PubMed DOI
Patra S, Bartošová-Sojková P, Pecková H, Fiala I, Eszterbauer E. Holzer AS. Biodiversity and host-parasite cophylogeny of Sphaerospora sensu stricto (Cnidaria: Myxozoa). Under revision in Parasit Vectors. PubMed PMC
Holzer AS, Bartošová-Sojková P, Born-Torrijos A, Lövy A, Hartigan A, Fiala I. Joint evolution of myxozoa and their alternate hosts: a recipe for success and vast biodiversity? Under revision in Mol Ecol. PubMed
Branch GM, Griffiths CL, Branch ML, Beckley LE. Two Oceans: A Guide to the marine life of southern Africa. 1st ed. Claremont, South Africa: David Philip Publishers; 1994.
Barta J, Martin D, Liberator P, Dashkevicz M, Anderson J, Feighner S, et al. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol. 1997;83(2): 262–271. PubMed
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14): 3059–3066. PubMed PMC
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12): 1647–1649. doi: 10.1093/bioinformatics/bts199 PubMed DOI PMC
Swofford DL. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts: 2003.
Stamatakis A. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics. 2006;22(21): 2688–2690. doi: 10.1093/bioinformatics/btl446 PubMed DOI
Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003;19(12): 1572–1574. PubMed
Rambaut A, Drummond AJ. Tracer v1.4; 2007. Available from: http://beast.bio.ed.ac.uk/Tracer.
Lodh N, Kerans BL, Stevens L. The parasite that causes whirling disease, Myxobolus cerebralis, is genetically variable within and across spatial scales. J Euk Microbiol. 2012;59(1): 80–87. doi: 10.1111/j.1550-7408.2011.00596.x PubMed DOI
Leigh JW, Bryant D. POPART: full-feature software for haplotype network construction. Method Ecol Evol. 2015;6(9): 1110–1116.
Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics. 2009;25(11): 1451–1452. doi: 10.1093/bioinformatics/btp187 PubMed DOI
Fu YX. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics. 1997;147(2): 915–925. PubMed PMC
Ramos-Onsins SE, Rozas J. Statistical properties of new neutrality tests against population growth. Mol Biol Evol. 2002;19(12): 2092–2100. doi: 10.1093/oxfordjournals.molbev.a004034 PubMed DOI
Tajima F. Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 1989;123(3): 585–595. PubMed PMC
Atkinson S, Bartholomew J. Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout (Oncorhynchus mykiss) and Chinook salmon (Oncorhynchus tshawytscha) correlate with internal transcribed spacer-1 sequence variation in the parasite. Int J Parasitol. 2010: 599–604. doi: 10.1016/j.ijpara.2009.10.010 PubMed DOI
Atkinson SD, Bartholomew JL. Spatial, temporal and host factors structure the Ceratomyxa shasta (Myxozoa) population in the Klamath River basin. Infect Genet Evol. 2010;10(7): 1019–1026. doi: 10.1016/j.meegid.2010.06.013 PubMed DOI
Atkinson SD, Jones SRM, Adlard RD, Bartholomew JL. Geographical and host distribution patterns of Parvicapsula minibicornis (Myxozoa) small subunit ribosomal RNA genetic types. Parasitology. 2011;138(8): 969–977. doi: 10.1017/S0031182011000734 PubMed DOI
Wuennemann H, Holzer AS, Pecková H, Bartošová-Sojková P, Eskens U, Lierz M. Repatriation of an old fish host as an opportunity for myxozoan parasite diversity: The example of the allis shad, Alosa alosa (Clupeidae), in the Rhine. Parasit Vectors. 2016;9. PubMed PMC
Henderson M, Okamura B. The phylogeography of salmonid proliferative kidney disease in Europe and North America. Proc R Soc Lond B Biol Sci. 2004: 1729–1736. PubMed PMC
Whipps C, El-Matbouli M, Hedrick R, Blazer V, Kent M. Myxobolus cerebralis internal transcribed spacer 1 (ITS-1) sequences support recent spread of the parasite to North America and within Europe. Dis Aquat Organ. 2004: 105–108. doi: 10.3354/dao060105 PubMed DOI
Whipps C, Kent M. Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Euk Microbiol. 2006: 364–373. doi: 10.1111/j.1550-7408.2006.00114.x PubMed DOI
Bartošová P, Fiala I. Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol Res. 2011;108(3): 573–583. doi: 10.1007/s00436-010-2100-y PubMed DOI
Bartošová P, Fiala I, Jirků M, Cinková M, Caffara M, Fioravanti ML, et al. Sphaerospora sensu stricto: Taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Mol Phylogenet Evol. 2013;68(1): 93–105. doi: 10.1016/j.ympev.2013.02.026 PubMed DOI
Bartošová-Sojková P, Hrabcová M, Pecková H, Patra S, Kodádková A, Jurajda P, et al. Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. Int J Parasitol. 2014;44(8): 565–577. doi: 10.1016/j.ijpara.2014.04.005 PubMed DOI
Kodádková A, Dyková I, Tyml T, Ditrich O, Fiala I. Myxozoa in high Arctic: Survey on the central part of Svalbard archipelago. Int J Parasitol Parasites Wildl. 2014;3: 41–56. doi: 10.1016/j.ijppaw.2014.02.001 PubMed DOI PMC
Holzer AS, Stewart S, Tildesley A, Wootten R, Sommerville C. Infection dynamics of two renal myxozoans in hatchery reared fry and juvenile Atlantic cod Gadus morhua L. Parasitology. 2010;137(10): 1501–1513. doi: 10.1017/S0031182010000247 PubMed DOI
Sitjà-Bobadilla A. Fish immune response to Myxozoan parasites. Parasite. 2008;15(3): 420–425. doi: 10.1051/parasite/2008153420 PubMed DOI
Gomez D, Bartholomew J, Sunyer JO. Biology and mucosal immunity to myxozoans. Dev Comp Immunol. 2014;43(2): 243–256. doi: 10.1016/j.dci.2013.08.014 PubMed DOI PMC
Poe S. Evaluation of the strategy of long-branch subdivision to improve the accuracy of phylogenetic methods. Syst Biol. 2003;52(3): 423–428. PubMed
Sanil NK, Chandran A, Shamal P, Binesh CP. Molecular and morphological descriptions of Ceratomyxa collarae n. sp and Ceratomyxa leucosternoni n. sp from marine ornamental fishes of Indian waters. Parasitol Res. 2017;116(2): 529–537. doi: 10.1007/s00436-016-5317-6 PubMed DOI
Yang ZH. On the best evolutionary rate for phylogenetic analysis. Syst Biol. 1998;47(1): 125–133. PubMed
von der Heyden S. Why do we need to integrate population genetics into South African marine protected area planning? Afr J Mar Sci. 2009;31(2): 263–269.
Blasco-Costa I, Poulin R. Host traits explain the genetic structure of parasites: a meta-analysis. Parasitology. 2013;140(10): 1316–1322. doi: 10.1017/S0031182013000784 PubMed DOI
Day JH. A monograph on the Polychaeta of Southern Africa. Part 2: Sedentaria. London: Trustees of the British Museum (Natural History); 1967.
Blamey LK, Branch GM. Habitat diversity relative to wave action on rocky shores: Implications for the selection of marine protected areas. Aquatic Conserv Mar Freshw Ecosyst. 2008. Available from: http://www.academia.edu/11425285/Habitat_diversity_relative_to_wave_action_on_rocky_shores_implications_for_the_selection_of_marine_protected_areas.
Adlard RD, Miller TL, Smit NJ. The butterfly effect: Parasite diversity, environment, and emerging disease in aquatic wildlife. Trends Parasitol. 2015;31(4): 160–166. doi: 10.1016/j.pt.2014.11.001 PubMed DOI
Unraveling the mystery of a myxozoan parasite of the trout: redescription of Chloromyxum schurovi